Alien Species and Evolution: The Evolutionary Ecology of Exotic Plants, Animals, Microbes, and Interacting Native Species

By George W. Cox

In Alien Species and Evolution, biologist George W. Cox reviews and synthesizes emerging information on the evolutionary changes that occur in plants, animals, and microbial organisms when they colonize new geographical areas, and on the evolutionary responses of the native species with which alien species interact.

The book is broad in scope, exploring information across a wide variety of taxonomic groups, trophic levels, and geographic areas. It examines theoretical topics related to rapid evolutionary change and supports the emerging concept that species introduced to new physical and biotic environments are particularly prone to rapid evolution. The author draws on examples from all parts of the world and all major ecosystem types, and the variety of examples used gives considerable insight into the patterns of evolution that are likely to result from the massive introduction of species to new geographic regions that is currently occurring around the globe.

Alien Species and Evolution is the only state-of-the-art review and synthesis available of this critically important topic, and is an essential work for anyone concerned with the new science of invasion biology or the threats posed by invasive species.

• Language: English
• Publisher: Island Press
• Release date: Apr 10, 2013
• ISBN: 9781597268356

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About Island Press

Island Press is the only nonprofit organization in the United States whose principal purpose is the publication of books on environmental issues and natural resource management.We provide solutions-oriented information to professionals, public officials, business and community leaders, and concerned citizens who are shaping responses to environmental problems.

In 2004, Island Press celebrates its twentieth anniversary as the leading provider of timely and practical books that take a multidisciplinary approach to critical environmental concerns. Our growing list of titles reflects our commitment to bringing the best of an expanding body of literature to the environmental community throughout North America and the world.

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Library of Congress Cataloging-in-Publication data.

Cox, George W., 1935–

The evolutionary ecology of exotic plants, animals, microbes, and interacting native species / George W. Cox.

p. cm.

Includes bibliographical references and index.

9781597268356

1. Introduced organisms--Environmental aspects. 2. Introduced animal—Evolution.

3. Exotic plants—Evolution. I. Title.

QH353.C69 2004

578.6’2—dc22

2003027299

British Cataloguing-in-Publication data available.

Design by Brighid Willson

Printed on recycled, acid-free paper e9781597268356_i0002.jpg

Manufactured in the United States of America

10 9 8 7 6 5 4 3 2 1

Table of Contents

About Island Press

Title Page

Copyright Page

Preface

Part I. - Basic Concepts of Alien Invasion and Evolution

1. - Alien Species and Accelerated Evolution

2. - Adaptation of Alien Species for Dispersal and Establishment

3. - Founder Effects and Exotic Variability

4. - Introduction Sources, Cryptic Species, and Invasion Routes

Part II. - Processes of Evolutionary Change and Adaptation

5. - Hybridization and Evolution of Exotics

6. - Hybridization and Transgenic Organisms

7. - Invasion Resistance of Native Communities

8. - Adaptation of Alien Species to New Habitats

Part III. - Evolutionary Interaction of Aliens and Natives

9. - Evolutionary Adaptation by Alien Herbivores

10. - Evolutionary Adaptation by Alien Predators and Parasites

11. - Adaptation of Alien Diseases to Hosts and Vectors

12. - Adaptation of Plants to Alien Herbivores and Diseases

13. - Adaptation of Native Herbivores to Alien Plants

14. - Adaptation of Animals to Alien Predators, Parasites, and Disease Agents

15. - Accumulation of Herbivores, Predators, and Parasites by Alien Species

Part IV. - Global Evolutionary Consequences of Alien Invasions

16. - Alien Species as Agents of Extirpation and Extinction

17. - Evolutionary Ecology of Alien Biological Control Agents

18. - Counteradaptation and Integration into the Biotic Community

19. - Dispersing Aliens and Speciation

20. - Permanently Altered Biotic Communities

Literature Cited

Glossary

Index

Island Press Board of Directors

Preface

The phenomena of biological invasions and rapid evolution have come together in the last decade to reveal a host of cases of rapid evolutionary change by alien species and the native species with which they interact. All groups of organisms—plants, animals, and microorganisms of all types—are involved. These examples of rapid evolution are of great interest to theoretical biologists, but they include many aspects of applied importance, as well. The potential for the spread of transgenes from plants of economic importance to wild and weed relatives is substantial. The same is true of transgenes introduced into populations of animals, especially those of importance in aquaculture and biological control. The growing number of species introduced for biological control also means a growing potential for ecological and evolutionary shifts that enable these agents to attack nontarget hosts. More generally, the mixing of genomes of alien and native species through hybridization increases the potential for the evolution of new invasive forms.

Despite the numerous, well-publicized cases of evolutionary shifts in human disease agents and the diseases and pests of agricultural plants and animals, the public at large remains largely unaware of the accelerated pace of evolution resulting from the massive introduction of species to new geographical regions. In particular, systems of governmental regulation of alien species tend to regard them as stable genetic entities. In education, the concept of evolution is treated as a controversial theory of the history of life on earth, rather than an on-going process of great relevance to human welfare.

Recognition of the importance of rapid evolution involving alien species culminates more than a half century of interest in the biology of introduced organisms. In 1958, in perhaps one of the most forward-looking publications in ecology, Charles Elton characterized introductions of animals and plants to new regions as one of the great convulsions of the world’s flora and fauna. In the book The Ecology of Invasions by Animals and Plants, he pioneered the field now known as invasion biology.

Although recognized as a classic analysis, Elton’s book did not immediately stimulate widespread research. In the 1970s, with growing concern about the endangerment and extinction of species, alien introductions were recognized as a major threat to native biodiversity. The risks to survival of island species and to the long-isolated biotas of regions such as New Zealand and Australia were recognized early. In the 1980s, research on the impacts of alien species expanded greatly, especially in North America, New Zealand, Australia, South Africa, and western Europe. Focused first on the impacts of aliens in terrestrial and freshwater environments, concern soon spread to the marine environment. With the availability of new techniques of genetic analysis in the 1990s, an explosion of research on population genetics and evolutionary change in alien species and interacting native species occurred. Research on alien species, and increasingly on their evolutionary biology, is now being pursued in almost all developed countries. Concern about alien species issues, however, still lags in many tropical countries.

The literature on alien species and their evolutionary biology is now growing at an enormous rate. The journal Biological Invasions (Kluwer Academic Publishers) began publication in 1999, and many other journals in both basic and applied areas of biology carry articles on aspects of alien species biology. The ecology and evolution of alien species are the subjects of frequent national and international meetings of scientists and environmental managers. Federal and state agencies are becoming increasingly active in efforts to control noxious alien species. Controversies relating to genetic engineering and biocontrol introductions have increased societal awareness of topics closely related to the evolutionary biology of alien species.

In this book, we will examine evolutionary issues of exotic species, drawing examples from all parts of the world and all major ecosystem types. The various technologies of analysis of the genetic composition of organisms and populations have enabled biologists to recognize evolutionary change in great detail. We have drawn from the numerous examples of recent rapid evolution that have been documented and that, more often than not, involve species that have invaded new regions within historical or postglacial time. We have also drawn from examples of natural invasions, many of which have occurred since retreat of the last continental glaciation. These give considerable insight into the patterns of evolution that are likely to result from the massive introduction of species to new geographical regions due to human activities.

To examine this rapidly developing field, in part I, we begin by examining several basic aspects of the evolutionary biology of alien species. These include the evolutionary dynamics of the dispersal and colonization processes that enable organisms to invade new areas and the patterns of genetic variability that are associated with these invasions. Within recent decades, powerful new techniques for characterizing genetic variability within populations have been developed. Among these are the well-known techniques of allozyme analysis and the more recent techniques of DNA fingerprinting and sequencing. These techniques are enabling breakthroughs in the detection of cryptic species, in describing the genetic structure of alien and source populations, in defining the number and location of establishment events, and in tracing the routes of alien species as they spread into new regions.

In part II, we examine basic relationships that determine the evolutionary potential of alien species in their new homes. These include the potential for hybridization with closely related native species or other aliens, the potential for gaining transgenes from genetically engineered species, the ability to overcome resistance of native communities to invasion, and the ability to adapt to basic abiotic and biotic conditions of the new environment. In the latter two challenges, the patterns of genetic variability that were considered in part I become key resources for adaptive evolution.

In part III, attention is turned to some of the most exciting examples of rapid evolution that have been documented in recent decades. These include the adaptation of alien species to the new native plant and animal species that they begin to exploit and the adaptation of native species to the new alien biotic agents that they encounter. Alien plants become suitable hosts for many native herbivores, whereas alien animals may exert selective influence either as enemies or as new prey or hosts. Alien plant and animal diseases or disease vectors also create strong new evolutionary pressures on many native species. For humans, understanding the evolutionary threats posed by alien species, as well as the capabilities of native species for their own evolutionary responses, is essential to sound environmental management.

Part IV provides an opportunity to look into the future, as alien invasions are a major component of global environmental change. Intentional and unintentional introductions of alien species are one of the principal causes of extirpation or extinction of native species. Additional introductions of alien species for biocontrol bring risks of similar impacts, especially because these species have the potential for evolutionary shifts in host use. In addition, alien species are becoming substantial components of biodiversity in almost all ecosystems, and it is thus essential to understand the potential of these ecosystems to assimilate them. Likewise, the potential for the aliens to stimulate speciation must be considered. Interacting with other aspects of global change, alien invasions are creating new community types and will play a major role in determining how ecosystems respond as global climates change. Humans have indeed altered the global evolutionary stage, and the evolutionary play has been speeded as a consequence.

I am indebted to many individuals for the help they have given in pulling together ideas and information from the extensive and scattered literature on evolutionary ecology of alien species. I especially thank the following individuals for reviewing one or more chapters and making valuable suggestions for improvement: Ellen Bauder, Amy C. Blair, Scott P. Carroll, Darla G. Cox, Melania E. Cristescu, Curtis C. Daehler, Margaret B. Davis, Jeffrey S. Dukes, Andrew P. Hendry, Bohun B. Kinloch, Jr., Christian Lexer, Svata M. Louda, Leroy McClenaghan, Megan McPhee, John Obrycki, Roger Peterson, Robert Ricklefs, Dolph Schluter, Kristina Schierenbeck, Craig A. Stockwell, Colin Townsend, David Truesdale, Thomas F. Turner, Kathy Williams, Lorne M. Wolfe, and Arthur Zangerl. I also thank the following individuals for helping me locate important literature: Janis Antonovics, Allison Colwell, Katie Beauchamp, Peter Bowler, Curtis C. Daehler, Jim Detling, Mark Dybdahl, Edwin D. Grosholz, Ronald Hedrick, Dan Herms, Stuart Hurlbert, Pat Johnson, James Juvik, Carolyn King, Lex Kraaijeveld, Svata Louda, Jim Mills, Gwen Mayo, Ray Newman, Jim Patton, Ian Payton, Sarah Reichard, Dave Rizzo, Dolph Schluter, Peter Sweetapple, and Lyndon Wester. Barbara Dean, executive editor for Island Press, gave many valuable suggestions for organization and presentation of the material.

GEORGE W. COX

Santa Fe, New Mexico

Part I.

Basic Concepts of Alien Invasion and Evolution

In this introductory series of chapters, we outline the basic issues of evolutionary biology of alien species and consider basic aspects of dispersal capabilities and genetic variability that are central to the study of evolutionary change by aliens.

In chapter 1, we begin our examination by reviewing the magnitude and economic impact of worldwide introduction of plants, animals, and microorganisms to new geographic regions. Patterns of rapid evolution associated with these introductions are then presented, and their general significance is described. The major evolutionary issues that will be examined in succeeding chapters are then outlined.

Chapter 2 begins our examination of specific evolutionary issues by considering the selective pressures that act on mechanisms of dispersal by species poised to invade new regions or exposed to the agents of long-distance transport that modern human technology has created. The adaptations and evolutionary responses that enable the individuals that reach new regions to become established and spread are also discussed.

In chapter 3, we consider the patterns of genetic variability that species bring with them to new regions. First, we review the most important techniques of assessing genetic variability in populations of species, both in their native source populations and in newly established alien populations. We then consider how the processes of introduction and establishment tend to influence the genetic structure of founder populations.

Finally, in chapter 4, we examine how analysis of the genetic composition of populations of alien species in their native regions and regions of introduction can reveal precise source regions and invasion routes. In addition, these analyses often are able to distinguish cryptic aliens—forms not previously recognized as alien or not clearly distinguished from each other in their morphology.

These introductory discussions prepare us to proceed to an examination of the processes by which evolutionary change and adaptation occur in alien species in their new homes.

1.

Alien Species and Accelerated Evolution

A growing appreciation that organic evolution, like mountain building, is an ongoing rather than simply historical process has stimulated an infusion of evolutionary thinking into mainstream ecology. Foremost among the factors that have fostered this development are reports of remarkable adaptive evolution known to have taken place in recent decades. . . .

—CARROLL ET AL. (2001)

Potato late blight (Phytophthora infestans) is a fungal disease of the Irish potato (Solanum tuberosum) and its relatives. The potato itself was domesticated in the Andean region of South America, whereas the blight fungus is believed to be native to the Toluca Valley of Mexico.The potato was introduced to Europe in the 1500s, and became a major food plant in Ireland and many other countries. A strain of the blight fungus somehow reached western Europe in the mid-1840s, where, coupled with weather conditions favorable to its development, it decimated potato crops. In Ireland, the almost total loss of the potato crop led to famine, in which 1.5 million people died and many more were forced to emigrate. Closely related strains of the fungus have since invaded all major potato-growing areas of the world. In the twentieth century, these strains have been more or less controlled by a combination of resistant potato varieties, fungicidal treatments, and sanitation.

Prior to the 1980s, strains of the blight fungus affecting potato and tomato (Lycopersicon esculentum) crops were of a single mating type, which reproduced asexually and showed little genetic variability. This genetic uniformity contributed significantly to the success of disease control. In the early 1980s, however, resurgence of late blight disease began to occur in the Old World, and by the late 1980s and early 1990s, severe outbreaks of the disease also affected potato crops in Canada and the United States (Fry and Goodwin 1997). These outbreaks were traced to new strains of late blight fungus that apparently originated in Mexico. The new strains were much more virulent and were resistant to one of the primary fungicides previously used to control late blight. These strains have already caused production losses measured in millions of dollars in parts of the Pacific Northwest.

Even more serious is the evolutionary potential created by these new forms of the late blight fungus. The new strains belong to the complementary mating type of the earlier fungus, so their arrival now makes possible sexual reproduction and resulting genetic recombination. Sexual reproduction has already been confirmed in several locations (Goodwin et al. 1998). New fungal strains that appear to be the result of recombination between different mating types have also been found on tomatoes in North Carolina (Wangsomboondee et al. 2002). Thus, the stage has been set for the rapid evolution of new genetic races of a fungus that is known to affect two of the world’s most important crops, potatoes and tomatoes, both of which are members of a plant family containing a host of other cultivated plants.

The Economic and Ecological Impact of Alien Species

Invasive alien species are now recognized throughout the world as one of the most serious ecological and economic threats of the new millennium (Pimentel 2002). Alien plants are reducing the productivity of agricultural crops, pastures, and rangelands and are disrupting many natural terrestrial ecosystems. In addition, alien plants are choking waterways and altering the function of freshwater and marine ecosystems. Many of these plants are now legally designated as noxious weeds. Alien animals are also altering the biotic structure of land, freshwater, and marine ecosystems and are pushing many native species toward extinction. Introduced disease agents are infecting crops, livestock, fish and game animals, timber trees, and horticultural plants. Increasingly, introduced diseases and their vectors are posing new threats to human health as well. The worldwide total of species introduced to new geographical regions by human agency probably approaches half a million species (Pimentel et al. 2001).

The direct and indirect economic costs of these invaders are enormous. In the United States alone, alien plants, animals, and microbes are estimated to cause economic losses of $137.2 billion annually (Pimentel et al. 2000), with estimates for agricultural losses worldwide reaching $248 billion (Pimentel et al. 2001). An additional $4.2 billion loss occurs in the United States due to alien forest insects and pathogens. Additional direct losses result from damage by aliens to fisheries, navigation, and industry. Still other costs are incurred in fighting alien species that are endangering native plants and animals. Invasions of natural ecosystems by alien species are degrading their unique aesthetic and recreational values.

Invasions of alien species are certain to continue, in spite of increasing awareness and prevention efforts. Much of this invasion is likely to occur as a result of increasing international trade and travel (Ewel et al. 1999). For the period from 1920 to 1990, for example, Levine and D’Antonio (2003) examined the relationship between value of foreign imports to the United States and the numbers of alien mollusks, plant pathogens, and insects becoming established.The most conservative model predicted that between 2000 and 2020 some three species of mollusks, five species of plant pathogens, and 115 species of alien insects are likely to become established in the United States. Less conservative models gave numerical predictions more than tenfold greater. Increased internal trade and traffic, including exchanges of organisms mediated via the Internet (see, e.g., Kay and Hoyle 2001), also mean that the spread of alien species within the United States and other countries will be great.

Alien Species and Contemporary Evolution

These threats, however, are only the tip of an ecological and evolutionary iceberg (Palumbi 2001). The worldwide introduction of alien species is leading to rapid evolutionary change in both alien species and the native species with which they interact. Contemporary in the sense that they occur over tens to hundreds of generations rather than millions of generations, these patterns of evolution are the result of profound human influences on the natural world (Stockwell et al. 2003). The introduction of alien species is interacting with habitat destruction and degradation, overexploitation of plants and animals in natural ecosystems, and global climatic change to create an evolutionary revolution. Patterns of rapid evolution involve all groups of organisms and all patterns of organismal interaction: plant-herbivore, prey-predator, and host-pathogen systems (Thompson 1998; Gilbert 2002). Far from slowing evolutionary change, humans have accelerated evolutionary processes.

Despite the serious impacts of alien species, their dynamic evolutionary potential has received little recognition. In particular, systems of regulation and management of these species have failed to recognize this potential. Alien species are classified as beneficial, harmless, or harmful, based on an evaluation of a limited sample of individuals at a particular time, with the usual result that they are either permitted or prohibited in commerce. Little attention is given to the risk of evolutionary change by alien species once they become established in a new region.

As we shall see, all species, both native and alien, are at all times subject to evolutionary pressures that may maintain an evolutionary status quo or may lead to gradual or rapid change in genetic characteristics. Freed, in many cases, from the constraints of gene flow from their parent population and from biotic pressures of former enemies, alien species acquire exceptional evolutionary opportunities. Because populations of alien species have become established in new physical and biotic environments, however, they are subject to altered selection pressures that are likely to bring about rapid evolutionary change. In their new environment, alien species may encounter close relatives from which they had been isolated geographically. Hybridization with these relatives may enhance their evolutionary potential. Furthermore, those aliens that become abundant and highly invasive impose strong new evolutionary pressures on the natives with which they interact.

The example of late blight of potatoes is only one of many cases in which alien species pose threats to human interests through their evolutionary potential. Strong anthropogenic selection pressures imposed by pesticides, antibiotics, and environmental pollutants such as heavy metals have long been known to induce resistance in plants, animals, and microbes. Numerous plants have shown rapid evolution of resistance to heavy metals in spoil heaps associated with mining activity (Macnair 1987). Literally hundreds of plants, animals, and disease organisms, many of them alien to the regions involved, have evolved resistance to pesticides (see, e.g., National Academy of Science 1986). More than 100 plants now show resistance to herbicides, with more being recorded annually.

The potential for alien species in general to show rapid evolutionary responses to other pressures, however, has been appreciated only in the last quarter century. Numerous examples of such evolutionary responses are now available. A recent survey (Reznick and Ghalambor 2001), for example, documented 34 studies of rapid evolution in response to agents other than pesticides, antibiotics, or pollutant chemicals. Most of these studies involve evolutionary changes following the introduction of a species to an environment with novel characteristics or to a new location. Some 18 of these studies reflected rapid evolutionary changes by alien species—organisms that had invaded or been introduced to new geographical areas.

The risks of unexpected evolutionary responses of alien species have been increased by the rapidly expanding technology of genetic engineering. This is particularly true for genes that confer tolerance by crop species and other beneficial organisms to herbicides or other pesticides, or that confer systemic resistance to pests or diseases. The majority of these genetically transformed species possess close relatives that are cropland weeds or wild ancestral species with the potential to evolve weed races. The possibility of escape of such genes via rapid evolutionary change demands the utmost caution in their introduction to open agricultural systems.

Appreciation is also growing that evolutionary change occurs within a community context, with change in individual species both being influenced by many other species and having impacts on other aspects of the community and ecosystem. This appreciation has led some to propose community genetics as a new subfield of science (Neuhauser et al. 2003). Whether or not such a branch deserves formal recognition, the fact is that rapid evolutionary change involving alien species and the natives with which they interact is proceeding on a very complex and influential ecological stage.

Adaptation of Alien Species for Dispersal

Dispersal is a basic life history process for all organisms and one of central importance to alien species. All species possess a life history stage—spore, seed, egg, larva, or mature organism—that is adapted in some way for transport by wind or water currents, attachment to animal carriers, or active locomotion to sites that may offer suitable habitat. Plants and animals adapted to ephemeral or disturbed habitats have long been known for their ability to disperse widely and colonize new, often isolated sites. During human evolution, such species have proven to be well adapted to the habitats created by human activity. Many have followed humans as they migrated to new areas and often refined their life history traits to take advantage of humans, both as creators of habitat and as agents of dispersal. Such species are preadapted to spreading rapidly once they have been introduced to a new geographical region.

Many species have taken advantage of wheeled vehicles, seagoing ships, and airplanes as agents of transport, enabling them to cross major geographical barriers. Many of these species, especially plants, have been carried deliberately to new regions (see, e.g., Mack and Erneberg 2002), but others have hitchhiked. Modern systems of travel and commerce have become strong agents of selection for altered modes of reproduction and dispersal.The intimate association of weeds and other pests with crops and domestic animals, for example, is favored not only by the care that humans give to these domesticated species, but also by the enhanced probability that weed and pest progeny will be transported to new world regions (Gould 1991). Natural selection is constantly acting to fine-tune adaptations for dispersal by natural and human agency (Dieckmann et al. 1999).

Adaptation of Alien Species to New Environments

Alien species show diverse patterns of evolutionary adaptability when they arrive in new geographical regions. Each has a particular pattern of genetic variability that influences its potential for evolutionary change. In some cases, variability may be very limited due to the small number of individuals in the founding population. Genetic drift in small initial populations may further reduce variability by genetic bottlenecking. The genetic composition of a new population may be a biased sample of variability in the source population, the so-called founder effect.Thus, evolutionary responses may be constrained by lack of variability in many cases.

On the other hand, many colonizers, especially those of early successional or disturbed habitats, arrive with high phenotypic and genetic adaptability. Founder populations of crop weeds and arthropod pests may consist of many individuals, carrying much of the variability of their source populations.The potential for such species to evolve races adapted to local conditions has long been recognized (Baker 1974). Aquatic organisms, carried in large numbers in ballast water of cargo ships, may also possess high genetic variability. Many other aliens, especially plants, have been introduced deliberately and in abundance, and their high genetic variability is guaranteed by multiple introductions and sources.

Alien species may also acquire genetic variability after their arrival. Many weedy plants, for example, are able to hybridize with closely related crop plants. Such hybridization may provide a source of new genetic variability, including transgenes that have been introduced by genetic engineering. In addition, complex patterns of hybridization may occur among species that were once isolated geographically but have been brought together in new regions or introduced to regions where they have close relatives among native species. In addition, the genetic composition of alien plants and animals is increasingly being influenced by multiple introductions that bring together genetic races from different parts of their native range. The hybrids of such races may show greater genetic variability than individual races in the native region.

Evolutionary adaptability is favored by other genetic features (Lee 2002). In particular, the fraction of additive genetic variance within the genome strongly influences adaptive capability. Additive genetic variance represents allelic variability through which selection can progressively modify a quantitative characteristic by increasing the frequency of particular alleles. Genetic loci that show additive genetic variation are termed quantitative trait loci. Epistasis, an interaction in which one gene influences the expression of another, can also facilitate rapid evolutionary change. The potential for chromosomal restructuring by inversions, translocations, duplications, or other changes that can influence gene action is another influential factor. The extent to which selection results in trade-offs of adaptive gain in one feature and loss of adaptation in another can also influence the capacity for evolutionary change.

For those aliens with favorable genetic variability, the particular habitat conditions and biotic pressures of the new environment often result in rapid evolutionary adjustments (Thompson 1998). Physical and chemical conditions differing from those of the native region select for adaptation to the new habitat. Biotic pressures due to predators, parasites, disease agents, and competitors are also altered. In some cases, these conditions are relaxed, favoring rapid population growth and high reproductive success by aliens. In these cases, selection may favor reallocation of resources from defense to growth and reproduction. In other cases, new biotic associates may be exploited for food or for pollination and seed dispersal. In time, many of the new associates may begin to act as predators, parasites, diseases, or competitors.

In general, the population growth that often follows colonization of a new geographical area is highly favorable for rapid evolution (Reznik and Ghalambor 2001). The success of an invader in spreading through a new region is often the product of its ability to adapt to the new conditions it encounters (García-Ramos and Rodríguez 2002). High dispersal ability may introduce populations to new areas to which they are poorly adapted and in which they fail to become established. In time, however, evolutionary adaptation by more slowly spreading populations may result in successful establishment in the same new areas.

Alien Species and Evolutionary Change by Natives

Evolutionary change flows outward from established alien populations, affecting the entire biotic community to some degree. Alien plants can alter conditions of the physical environment, changing physical conditions such as light intensity, chemical conditions such as soil salinity, and resource conditions such as nutrient availability. Use of resources by alien plants or animals can bring them into competition with natives. Alien predators, parasites, and disease agents establish complex new relationships with both natives and other aliens. The aliens themselves also constitute resources for native species to exploit. The presence of alien species thus leads to reorganization of the community food web and associated pressures of natural selection.

The establishment of an alien species thus creates a nucleus of accelerated evolution within the invaded community (Carroll and Dingle 1996).The evolution of the alien itself is accelerated, as new selective pressures act on it. As the alien population grows, its influence accelerates evolutionary change by native species. Selection may favor traits that reduce negative impacts of the alien or that enable native species to take advantage of the resources the alien provides. These adjustments by native species, known collectively as counteradaptations, in time integrate the alien into an altered biotic community.

Local communities and entire regional biotas invaded by aliens are thus permanently changed. The ubiquity and abundance of many alien species virtually precludes their eradication. Some, in addition, establish mutually beneficial interactions with native species, in some cases making their eradication undesirable. Even when alien species can be removed, a community of species that has been changed by evolution remains. Return of native species to an original evolutionary state is impossible, and a ghost of alien influence will remain. Alien invasions, alone and in combination with the influence of global climatic change, have already created new community types in many locations (Walther 2000).

Evolution by Alien Species and Global Change

On regional and continental scales, the effects of alien invasions are now being compounded by global climatic and habitat change (Mooney and Hobbs 2000). Global change has many aspects: climatic warming, atmospheric carbon dioxide increase, increased nitrogen deposition, increased ultraviolet radiation intensity, deforestation, desertification, chemical pollution, habitat disturbance and fragmentation, and loss of biodiversity. These aspects of global change are now beginning to strain the adaptation of many native species to the conditions to which they have long been closely adjusted. Most of these changes also make it easier for alien species to become established and spread. As a result, the frequency and intensity of biotic invasions are likely to be increased by global change (Lodge 1993b;Vitousek et al. 1997).

Global change compounds the evolutionary pressures acting on invading aliens. Where communities are in disequilibrium, natural selection is likely to favor plants and animals with short life spans, high dispersal abilities, rapid population growth capacities, opportunistic patterns of resource use, and high evolutionary adaptability (Barrett 2000). Fragmentation of habitats is likely to favor species with high dispersal and colonization capabilities (Barrett 2000). Thus, increasing numbers of rapidly evolving alien species are likely to alter the composition and dynamics of all of the world’s ecosystems.

Alien invasions possess the capacity to influence global climatic change (Mack et al. 2000). For example, the deliberate introduction of African tropical pasture grasses to the Amazon basin holds the potential to increase the importance of fire and inhibit the recovery of abandoned pasture areas to tropical forest. Flammable grasses would thus tend to convert forest areas into grasslands and savannas, with reduced biomass and transpiration. Such change would exacerbate the problem of atmospheric carbon dioxide accumulation as well as promote warmer and drier conditions throughout the region (fig. 1.1).

e9781597268356_i0003.jpg

Figure 1.1. Relationships of forest, grassland, fire, and climate as affected by the widespread introduction of African pasture grasses to the Amazon basin. The positive feedbacks from the initial influences of land clearing and introduction of exotic grasses promote the increased influence of fire, which increases the tendency for transformation of the landscape from tropical forest to grassland and savanna. (Reprinted with permission from R. N. Mack, D. Simberloff, W. M. Lonsdale,

H. Evans, M. Clout, and F. A. Bazzaz. 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10:689–710. © 2000 Ecological Society of America.)

Time Lags in Impacts of Aliens

Many alien species show a substantial time lag—years or decades—between initial establishment and the appearance of strong ecological impacts (Crooks and Soulé 1999). Time lags can exist for both ecological and evolutionary reasons (Kowarik 1995). For example, a time lag can result simply from the fact that a new alien species requires time to disperse into favorable habitat patches throughout a region and to build up populations capable of producing abundant seeds or offspring. At some point, it then becomes capable of a major population explosion and serious ecological impact. Initial populations may also suffer from low reproductive success because low population density restricts beneficial social interactions among individuals, the Allee effect (Lewis and Kareiva 1993). An Allee effect appears, for example, to account for the slow increase in the eastern population and range of the house finch (Carpodacus mexicanus ) between its introduction on Long Island, New York, in 1940 and the abrupt increase in its spread in about 1960 (Veit and Lewis 1996). Climatic shifts may also make environmental conditions favorable for invasive spread of a species long after its initial establishment.

On the other hand, an initial population may lack evolutionary adaptations that permit explosive population growth. After some time period, through genetic reorganization within the population, an evolutionary breakthrough may occur, enabling the alien to become an invasive species. A switch to earlier flowering, for example, has apparently enabled a ragwort (Senecio inaequidens) to become highly invasive in Europe (Kowarik 1995). Hybridization between species or between populations of a species from different source areas may be a major impetus for the evolutionary emergence of an invasive form after a time lag (Ewel et al. 1999; Ellstrand and Schierenbeck 2000).

Extirpation or Extinction of Native Species

Invasive alien species often cause the local extirpation and sometimes the complete extinction of native species. In particular, alien species introduced to insular environments such as islands, lakes, or rivers have caused numerous extirpations and extinctions in short periods of ecological time. Continental and oceanic areas are now beginning to experience these effects. Alien species may drive native species to extinction by competition, predation, or disease effects. Many native plants have suffered from hybridization and genetic swamping (Daehler and Carino 2001), as have some animals. The ability of native species to make the evolutionary adjustments necessary to prevent their extirpation or extinction varies greatly, and is a key concern of conservation biology.

The impact of alien species as agents of extirpation and extinction is of great concern because most habitats and regions of the world are being flooded by alien species in a very short period of ecological and evolutionary time. In most North American ecosystems, for example, more than 10% of species are now aliens, with more appearing every year. This rate of invasion exceeds by several orders of magnitude the invasion rate in pre-European time.

The extinction potential of this new era of alien invasions rivals the wave of extinction accompanying the colonization of the New World, Australia, New Zealand, and many oceanic islands by humans. More than half of the large mammals of North America disappeared at the end of the Pleistocene, coincident with the appearance and spread of human hunters through the New World. That human overkill is the probable mechanism of these extinctions is strongly supported by much evidence. Simulation of the population dynamics of the North American megafauna, species by species, confirms that human hunting is adequate to account for the extinction of almost all species (Alroy 2001).

In Australia, where 23 of 24 genera and 85% of species of large mammals disappeared about 46,000 yr ago, human colonization and its ecological impacts are among the most likely causes of extinction (Miller et al. 1999; Roberts et al. 2001). In New Zealand, recent data and analyses indicate that all 11 species of moas were hunted to extinction by humans in less than 100 yr, following arrival of Polynesians in the thirteenth century A.D. (Holdaway and Jacomb 2000). Throughout Melanesia, Micronesia, and Polynesia, colonization by humans between 1,000 and 30,000 yr ago resulted in extinction of more than 2,000 species of birds (Steadman 1995).

Evolutionary Responses of Native Species

One of the striking features of many invasions is a massive, early population outbreak that makes the alien form conspicuous and often highly destructive. In some species this outbreak may occur immediately after initial introduction; in others it occurs only after a delay of years, decades, or even a century. Following the outbreak, however, the population of the alien, as well as its ecological impact, may decline substantially. In many cases, native species also make ecological and evolutionary adjustments that shield them from the impacts of aliens. In addition, the population outbreak of the alien creates massive ecological and evolutionary opportunities for exploitation by members of the native community. Ecological responses may be rapid, as members of the native community learn to exploit the new community member as a food source and to avoid its direct detrimental influences. Later, evolutionary adjustments improve the ability of members of the native community to use the alien as a resource or to avoid the negative impacts of the alien.

Thus, over the long-term, evolutionary adjustments occur by members of the native community, and alien species may become integrated into the biotic assemblage. The sum of these responses or counteradaptations leads toward the reestablishment of a stable community. Stability, in this sense, implies that the alien has been accommodated at the level of dynamics of the landscape at large. That is, its regional population has stabilized, and its action in extirpation and extinction has ceased.

Not to be overlooked is the potential for pest species, native or alien, to evolve in response to selective pressures by deliberately introduced biological control agents. Although few such responses have been documented, most introduced biocontrol agents have been active only for a few years or decades. As we shall see, enough evidence has accumulated of this risk to require very detailed screening of prospective biocontrol agents and the inclusion of procedures to assess their evolutionary potential (Simberloff and Stiling 1996).

Alien Invasions and Speciation

In the short term, many biologists point out that the worldwide dispersal of alien species, combined with their role in extinction of species they encounter, is tending to homogenize the world’s biota, creating, in a sense, a New Pangaea (Rosenzweig 2001). An often overlooked evolutionary result of the spread of alien species, however, is the establishment of new, independent evolutionary populations in different geographical areas. Over the long term, divergence and speciation of these populations will to a degree offset the extinctions that occur in the shorter term.

As we shall see, patterns of evolution of alien species and the native species with which they interact are rapid, diverse, and often startling. New species are arising before our eyes by hybridization and divergent evolution. The patterns of rapid evolution seen in species expanding their ranges into new regions in many cases involve multiple adaptive traits and multiple genes (Reznick and Ghalambor 2001). The capacity for evolutionary change in areas where competition is low and the potential for rapid population growth high is considerable. Under these conditions, strong